Abstract
Non-coding transcription is an important determinant of heterochromatin formation. In Arabidopsis thaliana a specialized RNA polymerase V (Pol V) transcribes pervasively and produces long non-coding RNAs. These transcripts work with small interfering RNA to facilitate locus-specific establishment of RNA-directed DNA methylation (RdDM). Subsequent maintenance of RdDM is associated with elevated levels of Pol V transcription. However, the impact of DNA methylation on Pol V transcription remained unresolved. We found that DNA methylation strongly enhances Pol V transcription. The level of Pol V transcription is reduced in mutants defective in RdDM components working downstream of Pol V, indicating that RdDM is maintained by a mutual reinforcement of DNA methylation and Pol V transcription. Pol V transcription is affected only on loci that lose DNA methylation in all sequence contexts in a particular mutant, including mutants lacking maintenance DNA methyltransferases, which suggests that RdDM works in a complex crosstalk with other silencing pathways.
Highlights
RNA-directed DNA methylation (RdDM) is a plant transcriptional silencing pathway which targets transposable elements (TE), transgenes and repetitive sequences [1]
polymerase V (Pol V) transcribes long non-coding RNA and lncRNA is required for recognition of target loci by small interfering RNA (siRNA)-Argonaute complexes, which has been proposed to occur via siRNA-lncRNA base-pairing [9,11,15,16]
RdDM has been proposed to work as a self-reinforcing feedback loop [25], which predicts that mutants in components acting downstream of Pol V should affect the accumulation of Pol V transcripts
Summary
RNA-directed DNA methylation (RdDM) is a plant transcriptional silencing pathway which targets transposable elements (TE), transgenes and repetitive sequences [1] These loci are turned off by the establishment of repressive chromatin marks, including posttranslational histone modifications, nucleosome positioning and DNA methylation [2,3]. Pol V transcribes long non-coding RNA (lncRNA) and lncRNA is required for recognition of target loci by siRNA-Argonaute complexes, which has been proposed to occur via siRNA-lncRNA base-pairing [9,11,15,16]. The consequence of this recognition is recruitment of chromatin modifiers and heterochromatin formation [17,18,19]
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